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The Journal of Neuroscience, March 1, 2001, 21(5):1767-1778
Extrinsic Modulation and Motor Pattern Generation in a Feeding Network: a Cellular Study
Volko A. Straub and Paul R. Benjamin Sussex Centre for Neuroscience, University of Sussex, Falmer, Brighton, BN1 9QG, United Kingdom
Systems level studies have shown that the paired serotonergic cerebral giant cells (CGCs) of gastropod mollusks have important extrinsic modulatory actions on the central pattern generator (CPG) underlying rhythmic ingestion movements. Here we present the first study that investigates the modulatory actions of the CGCs and their released transmitter 5-HT on the CPG at the cellular level. In the snail, Lymnaea, motoneurons such as the B4, B8, and B4CL cells are part of the feeding CPG and receive serotonergic synaptic inputs from CGCs. These motoneurons were used to investigate the effect of serotonergic modulation on endogenous cellular properties of CPG neurons. Cells were isolated from the intact nervous system, and their properties were examined by pharmacological methods in cell culture. Motoneurons were also grown in coculture with CGCs to compare 5-HT effects with CGC stimulation. Three distinct modulatory effects of exogenously applied 5-HT/CGC activity were seen: all three motoneuron types were depolarized by 5-HT for prolonged periods leading to firing. Conditional bursting accompanied this depolarization in the B4/B8 cells, but not in B4CL cells. The frequency of the bursting was increased with increased CGC tonic firing. An increase in the size of postinhibitory rebound (PIR) occurred with 5-HT application in all three cell types, because of an increase in a CsCl-sensitive, hyperpolarization-activated inward current. Similar modulatory effects on membrane potential, endogenous bursting, and PIR properties could be observed in the intact nervous system and were necessary for motoneuron activation during feeding. Part of the systems gating and frequency control functions of the CGCs appear to be caused by these modulatory effects on feeding motoneurons.
Key words: Lymnaea; central pattern generator; neuromodulation; serotonin; conditional bursting; PIR; hyperpolarization-activated inward current; cell culture
Copyright © 2001 Society for Neuroscience 0270-6474/01/2151767-12$05.00/0
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